Microbiological evaluation of edible bovine by-products (intestine, lung, rumen meat, head flesh, heart, tongue, kidney and liver) commonly consumed in Assiut city, Egypt were determined by enumerating total viable bacterial count (TVBC), total enterobacteriacae count, yeast and mold contaminants and determine the presence of Salmonella spp. and E. coli O157:H7 organisms.
Int.J.Curr.Microbiol.App.Sci (2018) 7(1): 3449-3458 International Journal of Current Microbiology and Applied Sciences ISSN: 2319-7706 Volume Number 01 (2018) Journal homepage: http://www.ijcmas.com Original Research Article https://doi.org/10.20546/ijcmas.2018.701.406 Microbiological Evaluation of Some Edible Bovine By-products A.M Abd-El-Malek* and T El-Khateib Department of Food Hygiene (Meat Hygiene), Faculty of Veterinary Medicine, Assiut University, 71515 Assiut, Egypt *Corresponding author ABSTRACT Keywords Microbiological evaluation, Edible Bovine Byproducts, Salmonella spp., E coli 0157:H7 Article Info Accepted: 26 December 2017 Available Online: 10 January 2018 Microbiological evaluation of edible bovine by-products (intestine, lung, rumen meat, head flesh, heart, tongue, kidney and liver) commonly consumed in Assiut city, Egypt were determined by enumerating total viable bacterial count (TVBC), total enterobacteriacae count, yeast and mold contaminants and determine the presence of Salmonella spp and E coli O157:H7 organisms The obtained results showed that the mean TVBC of intestine, lung, rumen meat, head flesh, heart, tongue, kidney and liver were 9×10 6, 14×106, 6×107, 8×107, 7×106, 9×106, 7×106 and 5×106 cfu/g, respectively While, the mean enterobacteriacae count of intestine, lung, rumen meat, head flesh, heart, tongue, kidney and liver were 3×106, ×106, 3×107, 4×106, 7×105, 3×106, 3×106 and 3×106 cfu/g, respectively Furthermore, the mean total fungal count of intestine, lung, rumen meat, head flesh, heart, tongue, kidney and liver were 3×104, 8×104, 2×104, 6×104, 1×104, 7×104, 9×105 and 8×104 cfu/g, respectively Two S enteritidis could be isolated from intestine and lung samples One isolate of S typhimurium was detected in intestinal sample E coli 157:H7 contamination was found in intestine, lung, rumen meat and head flesh, respectively The results of this study show that edible bovine by-products are crosscontaminated by E coli 0157:H7, S enteritidis and S typhimurium and thus may pose potential risk for public health It is recommended that hygiene improvements are needed in the establishments selling edible bovine by-products to protect public health Introduction Edible meat by-products are a very economical source of high quality protein They are rich in mineral and vitamin contents (Oztan, 2005; Seong et al., 2014) In Egypt, the continuous increase in meat price lead the consumer to search for another suitable cheaper source of protein such as edible bovine by-products (Ockerman and Hansen, 2000) Edible bovine by-products are edible parts of internal organs also called variety meat or offal such as liver, kidney, heart, tripe and lung are eaten in large quantities by the population and most popular in Egypt especially in poor places Also, they are consumed in many countries all over the world like Turkey (Nazlı et al., 2005) Rumen meat, also, known as tripe is one of the important edible bovine by-products obtained from the first two chambers of a cattle's stomach: the rumen and the reticulum (Anna 3449 Int.J.Curr.Microbiol.App.Sci (2018) 7(1): 3449-3458 Anandh et al., 2012) Tripe is one of the high proteinnacious by product obtainable from slaughter house and is inexpensive with a distinguished taste (Ndeddy and Babalola, 2011) The intestine is a very long organ and is ideal for a casing of the sausage Mumbar means stuffed intestines made by stuffing the large intestine which are short and tubby, while those made from the small intestine are long and slender Due to readily available nutrients and poor hygienic conditions during handling, collection and processing, edible bovine by-products generally possess poor microbial quality (Selvan et al., 2007) As well as they have high loads of microorganisms (Oztan, 2005) They can be contaminated more frequently than animal carcasses by Salmonella (Little et al., 2008) Edible beef by-products have recently received significant attention worldwide (Im et al., 2016) However, studies evaluating the microbial safety of diverse edible beef by-products and specifically investigating contamination by pathogens that cause foodborne illnesses are rare The scarcity of the published information about the microbiological evaluation of edible bovine by-products obtained from different butcher's shops and street vendors Therefore, this study was carried out to enumerate total viable bacterial count, total Enterobacteriacae count and total fungal contaminants and to determine the presence of Salmonella spp and Escherichia coli O157:H7 in some edible bovine by-products commonly consumed in Assiut city, Egypt Materials and Methods Samples A total of 132 edible bovine by-products (included 36 intestine, 27 lung, 26 rumen meat, 11 head flesh, heart, tongue, ten liver and ten kidney) samples were collected randomly from different butchers open shops and street vendors in Assiut city, Egypt Samples were collected within hours postslaughter and during early morning, in order to minimize the microbial changes due to environmental temperatures and postslaughter timings Each sample was aseptically placed into a sterile plastic bag, labelled and transferred immediately to the laboratory for bacteriological analysis The selected internal organs were washed under running tap water to remove adhering blood, food remnants, feces, impurities, trimmed off of visible fats and connective tissues Rumen meat was cut into small chunks of about 2.5 cm (Anna Anandh et al., 2004) Microbial analysis (PHLS, 1998) The microbiological examinations of bovine by-products were assessed on the basis of Total Viable Bacterial Count (TVBC), total Enterobacteriacae count and total fungal count TVBC determined on standard plate count agar (OXOID, CM0463), Enterobacteriacae cultured on MacConkey agar (Biolife, CB 5502) and total fungal detected on Malt extract agar Base (HIMEDIA, M137) The standard procedure recommended by (ISI, 1980) was followed for microbial analysis with above respective media All plates were incubated under aerobic conditions at 36±1°C for 24- 72 hrs The mean number of colonies counted was expressed as colony forming units (cfu)/ per gram Detection and serological identification of Salmonella spp according to Kauffman (1974) and ISO (2002) Isolation and serology of E coli 0157:H7 as recommended by De Boer and Heuvelink (2000) and Kok et al., (1996) Data analysis was performed using SPSS v.16 statistical software package 3450 Int.J.Curr.Microbiol.App.Sci (2018) 7(1): 3449-3458 Results and Discussion Total Viable Bacterial Count (TVBC) The obtained results demonstrated in Table showed that the mean TVBC of intestine, lung, rumen, head muscles, trachea, heart, tongue, diaphragm, kidney and liver were 9×106, 14×106, 6×107, 8×107, 9×106, 7×106, 9×106, 1×107, 7×106 and 5×106 cfu/g, respectively The achieved results revealed that the TVBC of the edible bovine offal samples were higher than the permissible limits recommended by Egyptian Standard (E S, 2005) Similarly, in a related study conducted in Benha, Egypt, the mean value of TVBC of lung, liver, kidneys and heart were 4.01×107, 1.28× 107, 3.90×106 and 2.15×106 cfu/g, respectively (Gafer-Rasha, 2013) During slaughter and processing, all edible bovine tissues are subjected to contamination from a variety of sources within and outside animal The contaminating organisms are derived mainly from the hide of the animal and also comprise organisms that originate from feces (Datta et al., 2012) Enterobacteriaceae count According to the data recorded in Table 2, the mean enterobacteriacae count of intestine, lung, rumen, head muscles, trachea, heart, tongue, diaphragm, kidney and liver were 3×106, 3×106, 3×107, 4×106, 4×106, 7×105, 3×106, 2×107, 3×106 and 3×106 cfu/g, respectively These results revealed that the total enterobacteriacae count of the edible bovine offal samples were higher than the permissible limits sets by Egyptian Standard (E S, 2005) The achieved results in the current study revealed a higher counts of enterobacteriacae in different edible bovine offals compared with other authors such as Faten et al., (2013) who recorded that the mean values of total Enterobacteriaceae count/g of lung, liver and heart samples were 8.53×104, 3.96×104 and 9.17×103, respectively and Hafez et al., (1994) who found that Enterobacteriacae count of heart and liver was 2×10³ and 4×104, respectively Also, lower findings were reported by Ishak (1992) who found that Enterobacteriacae count 3.4×10³ cfu/g in abattoir samples; El-Seiiedy (1997) who found that Enterobacteriacae count of cattle liver was 4.28x104 and Ammar et al., (2012) who recorded that Enterobacteriacae count in examined beef liver was 2.2×103 The Enterobacteriaceae family is one of the main bacterial groups implicated in the contamination of bovine tripe Their presence in a food is an indication of improper hygienic measures (Gill and Landers, 2004) Total fungal count (TFC) Our results in Table found that the mean total fungal count of intestine, lung, rumen, head muscles, trachea, heart, tongue, diaphragm, kidney and liver were 3×104, 8×104, 2×104, 6×104, 12×104, 1×104, 7×104, 8×104, 9×105 and 8×104 cfu/g, respectively As E S (2005) does not establish safety limits for yeast and mould, it cannot be stated whether the values obtained here (1×1048×104 cfu g) imply a risk to human health On the other hand, there are studies with higher percentages such as that carried out by GaferRasha (2013), who reported that the mean value of total mycotic counts/g of lung, liver, kidneys and heart were 1.55x105, 2.97x105, 1.04x106 and 1.75x106 cfu/g, respectively Meanwhile, there is no fungus was found in the sample of meat and meat products except samples (Datta et al., 2012) The presence of yeast /mould in the food sample is due to it's disperse in the form of spores which are abundant in the environment and can be introduce through dust and soil (Apinis, 2003) Their presence in these food samples is a serious public health concern as these fungi may be associated with the production of mycotoxin (Makun et al., 2009) 3451 Int.J.Curr.Microbiol.App.Sci (2018) 7(1): 3449-3458 Salmonelle spp Regarding Salmonella spp., the results of this study demonstrated that two S enteritidis were isolated from intestine and lung (one sample from each) with percentage 3.7 and 2.7 %, respectively One strain of S typhimurium was isolated from one intestine sample with incidence 2.7% Moreover, S muenster (3.7%) was isolated from one lung sample The prevalence of Salmonella spp in edible bovine by-products was evaluated by many investigators In Germany Sinell et al., (1984) could isolate Salmonella with percentage of 68.9% and 28.9% in bovine lung and rumen meat samples, respectively The recovery rates of Salmonella spp were 10% for the liver and rumen meat samples and 20% for the brain samples obtained from local butcheries in another study conducted in Turkey Oflaz (2005) In a study performed by Akkaya et al., (2012), the detection rate of Salmonella spp was 16% in the liver and 4% in the kidney, tripe and brain samples Overall Salmonella prevalence (7.1%) in cattle offal from slaughterhouses in Korea was reported by Im et al., (2016) On the other hand, Ulutürk (1993) failed to detect salmonella in liver and rumen meat samples collected from abattoirs in Turkey Also, Keven and Ay (2003) reported the same findings from Turkey that none of the liver, tripe and brain samples from abattoirs were found positive The highest level of contamination of Salmonella spp was reported from the lung samples by Sinell et al., (1984) and from the liver samples by Samuel et al., (1980) Similarly, in our study the highest level of contamination with salmonella from intestine, lung and liver The presence of Salmonella spp in our samples may be due to multiple sources of contamination that crosscontamiante the offal during handling and processing post-slaughter and also reflects the intestinal bacterial load of slaughtered animals and hygienic standards of the abattoir (Akkaya et al., 2012) In addition, the sources of the Salmonella were probably the contents of the gastrointestinal tract Furthermore, there are numerous transmission routes for Salmonellosis, but the majority of the human infections are derived from consumption of contaminated foods especially those of animal origin (Saha et al., 2016) In our study, we failed to detect salmonella in rumen meat, head flesh, trachea, heart, tongue, diaphragms and kidney This is in accordance with the results of Selvan et al., (2007) who did not recover Salmonella from samples of retail meat products and Datta et al., (2012) who reported that none of the samples contained Salmonella and Shigella The absence of Salmonella in these offals samples indicate the quality of raw meat and other hygienic processing including the quality of the water used in washing and cleaning Other researchers could isolate Salmonella spp with different percentages such as Edris et al., (2013) who could isolate S typhimurium (4%) from lung samples and S typhimurium (4%) and S entertidis (4%) from liver samples and S entertidis (4%) from kidney samples, respectively Also, lower results were reported by Khalafalla et al., (1989) who examined 25 samples of bovine livers and could found S typhimurium (4%) From the achieved results of the present study, it declared that S enteritidis and S typhimurium are the most prevalent serotypes This result is compatible with Miller and Pegues (2005) who emphasized that S typhimurium and S enteritidis are the most common serotypes in the United States Furthermore, historically, S typhimurium is the most common agent of human food-borne disease, although in the last few decades S enteritidis has become more common (Braden, 2006) 3452 Int.J.Curr.Microbiol.App.Sci (2018) 7(1): 3449-3458 Table.1 Total viable bacterial count (TVBC) of examined edible bovine by-products (cfu/g) Samples No Min Max X- SE± Intestine Lung Rumen meat Head flesh Heart Tongue Kidney Liver 36 27 26 11 6 10 10 × 104 × 105 × 104 × 105 × 105 × 104 × 107 × 105 × 107 × 109 × 109 × 109 × 106 × 107 × 107 × 107 × 106* 14 × 106* × 107* × 107* × 106* × 106* × 106* × 106* 3.3 × 106 9.6 × 107 1.4 × 109 × 104 4.8 × 105 × 106 7.8 × 106 7.4 × 105 *Higher than Egyptian standards contamination load (ES, 2005) Min = minimum Max = maximum X - = mean value Table.2 Entrobacteriacae count of examined edible bovine by-products (cfu/g) Samples Intestine Lung Rumen meat Head flesh Heart Tongue Kidney Liver No 36 27 26 11 6 10 10 Min X- Max × 10 × 104 × 104 × 104 × 105 × 104 9.5 × 104 × 105 × 10 × 107 × 109 × 107 × 106 × 106 × 106 × 106 SE± 6* × 10 × 106* × 107* × 106* × 105* × 106* × 106* × 106* 1.2 × 106 1.4 × 106 4.9 × 107 1.5 × 106 × 105 × 105 4.6 × 105 3.8 × 105 *Higher than Egyptian standards contamination load (ES, 2005) Table.3 Total fungal count of examined edible bovine by-products (cfu/g) Samples No Min Max X- SE± Intestine 36 × 102 × 105 × 104 × 103 Lung 27 × 103 × 105 × 104 × 104 Rumen meat 26 × 102 × 105 × 104 1.9 × 104 Head flesh 11 × 103 × 105 × 106 2.2 × 104 Heart × 103 × 104 × 104 2.7 × 103 Tongue × 104 × 105 × 104 1.8 × 104 Kidney 10 × 103 × 105 × 104 × 104 Liver 10 × 104 × 104 × 104 6.2 × 103 3453 Int.J.Curr.Microbiol.App.Sci (2018) 7(1): 3449-3458 Table.4 Incidence of Entrobacteriaceae in the examined samples of edible bovine by-products Samples Intestine Lung Rumen meat Head flesh Heart Tongue Kidney Liver Total No E coli E coli Salmonella 0157:H7 0111:H4 spp No % No % No % 36 5.6 5.6 27 14.8 7.4 26 11.5 3.8 11 9.09 6 10 10 10 132 10 7.57 0.75 3.78 Shigella spp No % 5.6 14.8 26.9 18.8 16.6 10 17 12.8 Providencia rettgeri No % 2.8 0.75 The stomach of a cow is home to millions of microbes and therefore contamination of tripe derived from the rumen and reticulum is difficult to avoid especially during the evisceration process (Bensink et al., 2002; Ndeddy and Babalola, 2011) livers The isolated E coli is serotyped as O111, O128 and O26 Higher incidence achieved by Hassan and Osaman (2008) who could determine E coli O111 serovers (EHEC) in lung samples with percentage of 8% E coli 0157:H7 Shigella Concerning E coli, in the current study E coli 0157:H7 could be isolated from intestine (5.6%), lung (14.8%), rumen meat (11.5%) and head flesh (9.09%) samples, respectively In a related study, Asakura et al., (2012) screened 229 bovine offal products for the presence of Shiga toxin (stx) gene and found that eight (3.5%) were positive for E coli 0157:H7 Also, E coli O157:H7 was isolated from tongues (6.7%), liver (1.7%), omasa (5.0%) (Asakura et al., 2014) On the other hand, lower incidence (4.9%) of E coli O157:H7 in the rumen meat were recorded by Walker et al., (2010) In the present study, rumen meat was found contaminated with E coli O111:H4 serovers (3.8%) Nearly similar results obtained by Braden (2006) who could detect E coli O111:H4 serovers (EHEC) in lung samples (4%) and heart samples (4%), respectively and Bensink et al., (2002) who isolated E coli from 25 samples of cattle Regarding Shigella data outlined in Table showed that Shigella can be found in intestine, lung, rumen meat, head flesh, heart and kidney samples with an incidence of 5.6, 14.8, 26.9, 18.18, 16.6 and 10%, respectively The presence of Shigella usually indicates improper sanitary conditions and poor personal hygiene and is principally a disease – shigellosis – of humans, as well as other primates (Asghar et al., 2002) Providencia rettgeri Concerning Providencia rettgeri, the findings presented in Table revealed that Providencia rettgeri were isolated from only one out of 36 examined intestinal samples with an incidence of 2.8% The genus Providencia, belonging to the family Enterobacteriaceae, consists of spp., among these, P rettgeri may be associated with 3454 Int.J.Curr.Microbiol.App.Sci (2018) 7(1): 3449-3458 diarrhea (Yoh et al., 2005) Shima et al., (2016) could isolate P rettgeri in (8%) from retail meats in Thailand indicating that food animals, in particular meats, might be source of Providencia infection to human Control measures as prevention of contamination of abattoir environment by bacteria, application of ante-mortem and post-mortem inspection in abattoirs and implementation of proper hygienic conditions by personnel working in meat industry and cleaning/disinfection of the equipments and machines used for processing are important to minimize infections caused by these pathogenic microorganisms (Akkaya et al., 2015) The results obtained in the present study showed that the TVBC, total enterobacteriacae count of the edible bovine offal samples were higher than the permissible limits recommended by Egyptian Standards (ES, 2005) The prevalence of E coli 0157:H7 in the edible beef by-products is relatively high and the most common Salmonella serotypes were S enteritidis and S typhimurium so the presence of such food poisoning 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O157:H7 in gut contents of beef cattle at slaughter Foodborne Pathogen Disease 7, 249-55 Yoh, M., J., Matsuyama and Ohnishi, M et al., 2005 Importance of Providencia species as a major cause of travellers' diarrhoea Journal of Medical Microbiology 54, 1077-82 How to cite this article: Abd-El-Malek, A.M and El-Khateib, T 2018 Microbiological Evaluation of Some Edible Bovine By-products Int.J.Curr.Microbiol.App.Sci 7(01): 3449-3458 doi: https://doi.org/10.20546/ijcmas.2018.701.406 3458 ... presence of Salmonella spp and Escherichia coli O157:H7 in some edible bovine by-products commonly consumed in Assiut city, Egypt Materials and Methods Samples A total of 132 edible bovine by-products. .. Enterobacteriacea in edible offal Benha Veterinary Medical Journal 25, 77-87 Gafer-Rasha, W M 2013 Microbial evaluation of some edible offal in bovine carcasses Master Degree of Veterinary Science,... cause of travellers' diarrhoea Journal of Medical Microbiology 54, 1077-82 How to cite this article: Abd-El-Malek, A.M and El-Khateib, T 2018 Microbiological Evaluation of Some Edible Bovine By-products